Conservative estimates suggest that at least 3.9% of global vascular flora have been successfully naturalized in newly introduced regions (van Kleunen et al., 2015). Some species have since become invasive and spread rapidly, thereby exerting a negative impact on native biodiversity and ecosystem functions and services (Vila et al., 2011; Qi et al., 2014; Gallardo et al., 2016). Plant invasion is predicted to increase with human globalization (Seebens et al., 2015; van Kleunen et al., 2015). Elevated temperatures, altered precipitation, enhanced nitrogen (N) deposition, and increased atmospheric CO₂ concentrations are important environmental influences on ecosystems, ranging from the species level to ecosystem level (Stevens et al., 2004; Xu et al., 2014; Dieleman et al., 2015; Hautier et al., 2015; Xu et al., 2015, 2016). Additionally, plant invasion may be strongly affected by the major components of global environmental change (Bradley et al., 2010). The associations between plant invasion and global environmental change remain an emerging topic of interest in the fields of ecology and invasion biology (Bradley et al., 2010; Sheppard et al., 2014; Leishman and Gallagher, 2015; Seebens et al., 2015).

Global environmental changes could create novel environments and directly increase the availability of plant resources. Alien plants often exhibit broad environmental tolerance (Vilà et al., 2007; Hellmann et al., 2008; Scasta et al., 2015) and high phenotypic plasticity (Richards et al., 2006; Davidson et al., 2011; Si et al., 2014), facilitating their successful growth in novel environments with high resource availability (Davis et al., 2000; Pyšek and Richardson, 2007; Dostal et al., 2013). Numerous experimental studies have demonstrated that global environmental changes promote plant invasion. For instance, a recent meta-analysis comparing the growth performance response to global environmental changes (increased temperatures, increased precipitation, N deposition, and atmospheric CO₂ concentrations) between 74 invasive alien and 117 native plants found that these changes favor the performance of invasive alien plant species over that of native plants (Liu et al., unpublished). However, the mechanisms by which these global environmental change factors promote alien plant growth are yet to be established.

Interestingly, alien plant species classified within different functional groups (e.g., life forms and photosynthetic pathways) may show different responses to global environmental changes (Scasta et al., 2015). For example, the biomass of woody plants increases more than that of herbaceous plants in response to warming (Lin et al., 2010). C4 plants are more drought-tolerant and show favorable responses to CO₂ enrichment and warming (Lara and Andreo, 2011; Yamori et al., 2014). Moreover, many potentially important functional traits of species appear to promote the invasiveness of alien plants. To further explore this finding, a recent meta-analysis (van Kleunen et al., 2010) compared the pair-wise trait differences of 125 invasive and 196 non-invasive plant species. The study showed that invasiveness of alien plants is associated with performance-related traits (physiology, leaf area allocation, shoot allocation, growth rate, size, and fitness). Clarification of the responses to global environmental changes of functional groups (life forms and photosynthetic pathways) and different functional traits could therefore help determine how global changes facilitate alien plant growth.

Meta-analysis is an established tool that provides information to answer important ecological questions for organisms with different traits or belonging to diverse functional groups (Osenberg et al., 1997, 1999; Scasta et al., 2016). In the current study, we conducted a phylogenetically controlled meta-analysis using data from 111 published studies encompassing 129 alien species. Specifically, we compared the differences in response to global environmental changes across six categories of functional traits between woody and non-woody life forms and between C3 and C4 photosynthetic pathways of alien plants. The following research issues were addressed: (1) the extent of differences in plant functional groups (i.e., between woody and non-woody or C3 and C4 alien plants) in terms of response to increased temperature, precipitation, N deposition, and atmospheric CO₂ concentrations and (2) extent of variations in alien plant traits based on these global changes.

To determine the response of plant species level and functional groups to global environmental changes, we pooled effect sizes (weighted by inverse variance) and corresponding variances per species of each study in Data-I to generate a new database, Data-II. In the analysis of Data-II without considering functional groups, alien plants showed overall significantly positive responses to environmental change (LnR = 0.304, 95% CI = 0.209–0.399, n = 218; Figure 1) as well as each of the four global environmental change factors, i.e., elevated temperature (LnR = 0.235, 95% CI = 0.108–0.361, n = 53; Figure 1), precipitation (LnR = 0.321, 95% CI = 0.197–0.444, n = 38; Figure 1), N deposition (LnR = 0.421, 95% CI = 0.286–0.557, n = 44; Figure 1), and atmospheric CO₂ concentration (LnR = 0.274, 95% CI = 0.164–0.384, n = 83; Figure 1).

In the analysis for Data-II considering life forms or photosynthetic types of species, the average plant responses were not affected by life forms (Q_M = 0.043, df = 1, p = 0.835; Table 1, Figure 2) or photosynthetic type (Q_M = 1.499, df = 1, p = 0.221; Table 1, Figure 2). In a separate analysis for individual environmental factors, no significant differences were observed between woody and non-woody or C3 and C4 alien plants in response to elevated precipitation, N deposition, and atmospheric CO₂ concentration (Table 1, Figure 2). However, C4 alien plants exhibited a more positive response to elevated temperature than C3 alien plants (Q_M = 0.266, df = 1, p = 0.034; Table 1; Figure 2).

In the analysis of Data-I considering the differences among six trait categories, global environmental changes had significant positive effects on plant growth rate, physiology, shoot allocation, and size (Table 2, Figure 3). However, the patterns were different for each global environmental change factor. Warming induced significant positive responses in plant growth rate and size (Table 2, Figure 3B), increased precipitation affected plant fitness, growth rate and size (Table 2, Figure 3C), increased N deposition influenced plant fitness, growth rate, physiology, shoot allocation, and size (Table 2, Figure 3D), and CO₂ enrichment promoted plant growth rate, physiology, and size (Table 2, Figure 3E).

Alien plants are proposed to benefit from global environmental changes. Data from the current phylogenetically controlled meta-analysis suggested that alien plants show a positive plastic response in performance to the four environmental change components assessed, and furthermore, are not dependent on life forms and photosynthetic types. Notably, however, C4 plants showed a more positive response to warming than C3 plants. Our findings provide further evidence that all four global environmental change components promote the growth of alien plants mainly by increasing growth rate and size, although the patterns of effects on different alien plant traits vary among these components.

The finding of positive plastic responses to components of environmental change by alien plants is in line with data from our recent meta-analysis comparing the growth performance response to these four factors between invasive alien and native plants (Liu et al. unpublished). Recently, Sorte et al. (2013) published a meta-analysis on the responses of alien and native organisms to climate change and showed that terrestrial organisms show a positive performance response to CO₂ enrichment and elevated precipitation. However, warming had no significant effects. One possible explanation for the discrepancies between the results is that Sorte et al. (2013) evaluated the responses of both plants and animals to environmental change and did not correct for phylogenetic non-independence of the species analyzed (Chamberlain et al., 2012). Furthermore, we found that C4 plants responded more positively than C3 plants under warming conditions. This could be explained by the fact that unlike C3 plants, C4 plants generally originate from warm climates (Sage and Monson, 1998; Lara and Andreo, 2011) and the plastic ability of photosynthesis is also greater for C4 than C3 plants (Yamori et al., 2014). Moreover, C4 plants show better nitrogen and water efficiency than C3 plants at high temperatures (Yamori et al., 2014). Although C4 plants are significantly more efficient in using CO₂, we observed similar responses in both C4 and C3 plants under CO₂ enrichment, which may be attributable to the fact that CO₂ enrichment enhances the growth of C4 plants specifically under drought stress conditions (Xu et al., 2014).

Global environmental changes have significant positive effects on alien plant growth rate and size, as revealed by both joint and separate analyses. In our experiments, alien plants displayed increased growth rates and sizes in response to the four factors analyzed. High growth rate is frequently positively associated with high annual biomass production (trait category “size”) (van Kleunen et al., 2010). As expected, we observed consistency in responses between the growth rate and size categories. Generally, alien plant species tolerate a broad range of environmental conditions (Vilà et al., 2007; Hellmann et al., 2008) and display higher potential growth rates and sizes than native plant species under current global environmental conditions (van Kleunen et al., 2010; Davidson et al., 2011), which may explain why some alien plants outperform native plants. The global environmental change-induced positive responses of both trait categories of alien plants may become more advantageous, thereby facilitating their growth to a higher extent than that of native plants in the future. Moreover, specific factors, such as elevated precipitation and increased N deposition, could increase the fitness of alien plants, further contributing to their success under global environmental change conditions.

Global environmental changes had a significant positive effect on shoot allocation of alien plants in the joint analysis. However, only increased N deposition exerted a significant positive effect in the separate analysis, consistent with data from earlier studies (Poorter and Nagel, 2000; Drenovsky et al., 2012; Poorter et al., 2012; Freschet et al., 2015). The functional equilibrium hypothesis (Brouwer, 1962, 1963) suggests that plants shift their allocation toward roots when below-ground resources are low. Generally, plants are limited in productivity by nutrient availability, particularly N and/or P (Vitousek and Howarth, 1991; Fisher et al., 2012). Increased N deposition could change the resource limitation of alien plants from below- to above-ground, leading to a shift in allocation to shoots. Compared with other global environmental change factors, only increased N deposition exerted significant positive effects on all trait categories, except leaf area allocation. This finding may be attributable to the invasive nature of most of the alien species used in the analysis. According to Dostal et al. (2013), alien plants introduced from more N-rich habitats are more invasive and thus more likely to adapt to environments with high N levels.

Global environmental changes had a significant positive effect on the physiology of alien plants in the joint analysis. However, only increased N deposition and CO₂ enrichment exerted significant positive effects in the separate analysis. While elevated temperature and precipitation positively affected the physiology of alien plants, the effects were not significant. Our results contradict those of a recent meta-analysis of 197 studies by Liang et al. (2013), which showed that warming has overall positive effects on plant photosynthesis. Generally, most plants adjust their photosynthetic characteristics to temperature acclimation and the photosynthesis-temperature curve is often symmetrical or bell-shaped (e.g., Yamori et al., 2010, 2014). The discrepancy between our findings and those of other studies may be attributed to the different warming treatments among experiments and temperature sensitivities of various plant species (Llorens et al., 2004). Furthermore, water availability is an important factor limiting plant physiology, and many studies have shown that plant species have higher photosynthetic rates under increased than ambient precipitation. The non-significant effect in this meta-analysis is most likely attributable to the low statistical power.

To facilitate comparisons with other global change factors in the present meta-analysis, we included a number of studies that considered drought treatment as elevated precipitation by changing the control and treatment levels. However, precipitation levels are variable among different regions. For example, precipitation patterns associated with global changes are predicted to vary, with some areas receiving more precipitation than the others in the US (Naz et al., 2016). Therefore, we performed post hoc analyses for the different subsets considering whether water availability in a study increased or decreased, compared to the ambient levels. We observed opposite effects of increased and decreased precipitation on alien plants. Specifically, increased precipitation promoted growth whereas decreased precipitation inhibited growth (Supplementary Figure S1), suggesting that invasiveness of alien plants decreases when the climate becomes drier.

Many alien plants do not simply disperse on their own, but are spread by humans or as a result of changing environments (White et al., 2013; Scasta et al., 2015). The present meta-analysis has provided a quantitative summary of data showing that global environmental changes create favorable environmental conditions that could promote the growth of alien plants. Thus, alien plants have greater ecological effects and cause potential damage to ecosystem functions and services with global environmental changes (Kettenring and Adams, 2011; Vila et al., 2011; Scasta et al., 2015). However, since only 24 of the 111 total studies included in our meta-analysis manipulated more than one global environment change factor, we summarized the patterns of alien plant responses to individual components. Many of these components change simultaneously, and combination of more than one may exert different effects on plant performance related to a single component (Dukes et al., 2005; Xu and Zhou, 2006; Bloor et al., 2010; Dieleman et al., 2012). Further large-scale empirical studies are essential to determine the interactive effects of environmental change components on alien plant performance.

Data from our phylogenetically controlled meta-analysis showed that elevated temperature, precipitation, N deposition, and atmospheric CO₂ concentration promote alien plant growth. Elevated temperature had a more positive effect on C4 than C3 plants, indicating that C4 alien plants have higher potential for invasion than C3 plants under future global warming conditions. While different global environmental change factors affected distinct functional traits of alien plants, all four components promoted growth predominantly by increasing growth rate and size, potentially representing one of the mechanisms used by alien plants to adapt and facilitate successful growth under ever-changing environmental conditions.

YL designed this study. YL, JJ, and ZD compiled the data. YL and JJ analyzed the data. JJ drafted the manuscript with major inputs from YL as well as contributions from ZD and FL.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.